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An Updated Review of Ciguatera Fish Poisoning: Clinical, Epidemiological, Environmental, and Public Health Management

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An Updated Review of Ciguatera Fish Poisoning: Clinical, Epidemiological, Environmental, and Public Health Management marine drugs Review An Updated Review of Ciguatera Fish Poisoning: Clinical, Epidemiological, Environmental, and Public Health Management Melissa A. Friedman 1,*, Mercedes Fernandez 2, Lorraine C. Backer 3, Robert W. Dickey 4, Jeffrey Bernstein 5,6, Kathleen Schrank 5, Steven Kibler 7, Wendy Stephan 6, Matthew O. Gribble 8, Paul Bienfang 9, Robert E. Bowen 10, Stacey Degrasse 11, Harold A. Flores Quintana 12, Christopher R. Loeffler 12, Richard Weisman 6, Donna Blythe 13, Elisa Berdalet 14, Ram Ayyar 15, Danielle Clarkson-Townsend 8, Karen Swajian 11, Ronald Benner 12, Tom Brewer 16 and Lora E. Fleming 17 1 Mount Sinai Medical Center, Miami Beach, FL 33140, USA 2 Department of Psychology and Neuroscience, Nova Southeastern University, Fort Lauderdale, FL 33314, USA; [email protected] 3 National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA 30341, USA; [email protected] 4 Marine Science Institute, University of Texas at Austin, Port Aransas, TX 78373, USA; [email protected] 5 Jackson Memorial Medical Center, Department of Medicine, University of Miami, Miami, FL 33136, USA; [email protected] (J.B.); [email protected] (K.S.) 6 Florida Poison Information Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA; [email protected] (W.S.); [email protected] (R.W.) 7 NOAA-National Ocean Service, Center for Coastal Fisheries and Habitat Research, Beaufort, NC 28516, USA; [email protected] 8 Department of Environmental Health, Emory University Rollins School of Public Health, Atlanta, GA 30322, USA; [email protected] (M.O.G.); [email protected] (D.C.-T.) 9 Oceanography Department, University of Hawaii, Honolulu, HI 96822, USA; [email protected] 10 School for the Environment, University of Massachusetts Boston, Boston, MA 02125, USA; [email protected] 11 Food and Drug Administration, College Park, MD 20740, USA; [email protected] (S.D.); [email protected] (K.S.) 12 Food and Drug Administration, Dauphin Island, AL 36528, USA; harold.fl[email protected] (H.A.F.Q.); christopher.loeffl[email protected] (C.R.L.); [email protected] (R.B.) 13 Private Practice, Miami, FL 33133, USA; [email protected] 14 Institut de Ciències del Mar (CSIC), 08003 Barcelona, Spain; [email protected] 15 Department of Neurology, University of Miami, Miami, FL 33136, USA; [email protected] 16 Northern Institute, Charles Darwin University, Darwin 0909, Australia and Australian Institute of Marine Science, Darwin 0811, Australia; [email protected] 17 European Centre for Environment and Human Health, University of Exeter Medical School, Truro, Cornwall Tr1 3HD, UK; l.e.fl[email protected] * Correspondence: [email protected]; Tel.: +305-803-9008 Academic Editor: Lucio G. Costa Received: 7 December 2016; Accepted: 13 February 2017; Published: 14 March 2017 Abstract: Ciguatera Fish Poisoning (CFP) is the most frequently reported seafood-toxin illness in the world. It causes substantial human health, social, and economic impacts. The illness produces a complex array of gastrointestinal, neurological and neuropsychological, and cardiovascular symptoms, which may last days, weeks, or months. This paper is a general review of CFP including the human health effects of exposure to ciguatoxins (CTXs), diagnosis, human pathophysiology of CFP, treatment, detection of CTXs in fish, epidemiology of the illness, global dimensions, prevention, Mar. Drugs 2017, 15, 72; doi:10.3390/md15030072 www.mdpi.com/journal/marinedrugs Mar. Drugs 2017, 15, 72 2 of 41 future directions, and recommendations for clinicians and patients. It updates and expands upon the previous review of CFP published by Friedman et al. (2008) and addresses new insights and relevant emerging global themes such as climate and environmental change, international market issues, and socioeconomic impacts of CFP. It also provides a proposed universal case definition for CFP designed to account for the variability in symptom presentation across different geographic regions. Information that is important but unchanged since the previous review has been reiterated. This article is intended for a broad audience, including resource and fishery managers, commercial and recreational fishers, public health officials, medical professionals, and other interested parties. Keywords: ciguatera fish poisoning; ciguatoxin; harmful algal bloom; algae; seafood poisoning; Gambierdiscus; diagnosis; treatment; human health; natural toxins; climate change; environmental change; food poisoning; neuropsychology; neurology; neurotoxin 1. Introduction Ciguatera Fish Poisoning (CFP) is the most commonly reported natural marine toxin related illness globally [1]. It is characterized by gastrointestinal, neurologic, and cardiac symptoms. Humans contract CFP by eating finfish containing the naturally occurring toxins, ciguatoxins (CTXs). CFP is not due to the mishandling of fish and is not prevented by any particular storage, preparation, or cooking methods. The CTXs are tasteless, colorless, odorless, heat and acid stable, and stable for at least six months at commercial freezing temperatures [2,3]. Thus, prevention and management of CFP require a multidisciplinary approach. CTXs and their precursors are produced by microscopic algae known as dinoflagellates, in the genus, Gambierdiscus. These dinoflagellates are bottom-dwelling [4] and are typically found attached to seaweeds, living and dead corals, and other substrates (i.e., surfaces) in shallow tropical and subtropical waters. Due to Gambierdiscus’ requirements for light and substrate, CTX production occurs in shallow coastal habitats (e.g., reefs, atolls). Oceanic fish whose nutrition is derived from pelagic (i.e., in open sea waters and away from the shore) food webs rather than shallow/coastal food webs are less susceptible to the accumulation of CTXs. Table1 provides examples of fish commonly associated with CFP. Table 1. Examples of Common Ciguatoxic Fish Species [5] (Common name of the family in English (and Latin); also, some genera (g.) are cited as examples.) Moray eel (Muraenidae) Barracuda (Sphyraenidae) Grouper (Serranidae) Jacks (Carangidae) Amberjack (Carangidae, g. Seriola) Snapper (Lutjanidae) Surgeon fish (Acanthuridae) Parrot fish (Scaridae) Wrasses (Labridae) Hogfish (Labridae, g. Lachnolaimus) Narrow barred mackerel (Scombridae, g. Scomberomorus) Spanish mackerel (Scombridae, g. Scomberomorus) Trevally (Carangidae, g. Caranx) Triggerfish (Balistidae) Note: Various other examples of ciguatoxic fish are reported around the world [6–15]. Mar. Drugs 2017, 15, 72 3 of 41 CTXs are transferred and metabolized through the food web, as Gambierdiscus cells are ingested by herbivorous fish, which are then consumed by piscivorous fish, both of which are then consumed by humans. It is believed that CTXs are bioaccumulated and concentrated, such that fish higher in the food web tend to contain the highest CTX concentrations [16–20]. However, recent studies from French Polynesia and Hawaii indicate a general lack of relationship between fish size and ciguatera toxicity for many species and families of fish, suggesting that fish size alone is not an adequate predictor of toxicity [21,22] at least in those regions. While Gambierdiscus is known to produce two main types of toxins, the water-soluble maitotoxins and the lipid-soluble CTXs, maitotoxins have no proven role in CFP [23,24]. Examples of the CTX structures from Gambierdiscus spp. and their closely related isomers and congeners, isolated from fish collected in the Pacific Ocean [25,26], Caribbean Sea [2,27] and Indian Ocean [28], are summarized in Yasumoto and Murata (1993) [29] as well as Dickey (2008) [30], and the references therein. Historically, CFP was associated with isolated island communities that relied heavily on subsistence fishing for their food supply [31,32], but the geographic reach of CFP has expanded due to international seafood trade and travel [33–37]. In addition, people consuming fish from areas previously free of CFP may be at risk when such areas become prone to CFP [38–40] due to changes in the aquatic environment. It has also been speculated that CTXs may accumulate in farm-raised fish not typically associated with CFP via feed composed of wild fish contaminated with CTX [41]. Thus, the human populations that need to be incorporated into CFP risk assessments include not only those in endemic areas, but also tourists and recreational fishers traveling to endemic areas, transients (e.g., ships’ crews visiting endemic areas), and people in other regions consuming fish imported from endemic areas [36,38,42–44]. It is notable that the fish commonly associated with CFP are among the top selling species in many markets. In Florida in 2013, for instance, certain species of Grouper (Serranidae family), Snapper (Lutjanidae family), Mackerel (Scombridae family), and Jacks (Carangidae family) were among the top 20 types of finfish sold [45]. In 2014, 41.3 metric tons of barracuda were sold in Florida [46,47], a significant seafood market, given that barracuda is broadly viewed as ha ving an extremely high potential to be ciguatoxic. This highlights the importance of awareness on the part of the public and healthcare professionals, as well as the development of effective CFP risk management systems on a local to global scale. 2. Human Health Effects and Diagnosis The diagnosis of CFP is based on the recent fish-eating history of the patient(s), clinical presentation, and whenever possible,
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